The Ecological Importance of Horseshoe Crabs in Estuarine and Coastal Communities: A Review and Speculative Summary

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1 The Ecological Importance of Horseshoe Crabs in Estuarine and Coastal Communities: A Review and Speculative Summary Mark L. Botton Abstract Beyond their commercial importance for LAL and bait, and their status as a living fossil, it is often asserted that horseshoe crabs play a vital role in the ecology of estuarine and coastal communities. How would the various ecological relationships involving horseshoe crabs be affected if these animals were no longer abundant? Attempts to understand and generalize the ecological importance of horseshoe crabs are hampered by several constraints. We know relatively little about the ecology of juvenile horseshoe crabs. Most ecological studies involving adult Limulus polyphemus have been conducted at only a few locations, while much less is known about the three Indo-Pacific species. Furthermore, we are attempting to infer the ecological importance of a group of animals whose numbers may have already declined significantly (the so-called shifting baseline syndrome ). Horseshoe crab shells serve as substrate for a large number of epibionts, such as barnacles and slipper limpets, but the relationships between these epibionts and horseshoe crabs appear to be facultative, rather than obligatory. Horseshoe crabs are dietary generalists, and adult crabs are ecologically important bivalve predators in some locations. The most notable predator prey relationship involving horseshoe crabs is the migratory shorebird horseshoe crab egg interaction in Delaware Bay. After hatching, the first and second instars are eaten by surf zone fishes, hermit crabs, and other predators. Virtually nothing is known about predator prey relationships involving older juveniles, but adult L. polyphemus are important as food for the endangered loggerhead turtle, especially in the mid-atlantic region. 1 Introduction As with discussions about the significance of preserving global biodiversity, the rationale for conserving horseshoe crabs is often condensed into monetary terms. On these grounds, the considerable economic value of horseshoe crabs for lysate, M.L. Botton (*) Department of Natural Sciences, Fordham College at Lincoln Center, 113 West 60th Street, New York 10023, USA botton@fordham.edu J.T. Tanacredi et al. (eds.), Biology and Conservation of Horseshoe Crabs, DOI / _3, Ó Springer ScienceþBusiness Media, LLC

2 46 M.L. Botton bait, and ecotourism makes a very forceful case for the need for sustainable horseshoe crab populations (e.g., Berkson and Shuster 1999; Manion et al. 2000). However, just as the preservation of ecological diversity has ecological benefits that are not easy to transpose into dollars, horseshoe crabs may have underappreciated roles in the ecosystem that need to be part of the discourse about their value. The objective of this chapter is to review the ecological role of horseshoe crabs in estuarine and coastal environments with the goal of better understanding some of these additional ecological benefits. One way of envisioning the ecological roles (as suggested to me by Jane Brockmann) is to project how the functioning of ecosystems would differ if horseshoe crabs were absent or extremely rare. To accomplish this analysis, I subdivide the ecological role of horseshoe crabs into three parts: the importance of horseshoe crabs as predators, their importance as prey, and their importance as hosts for epibionts. In reviewing the literature, it became clear that there were constraints to the inferences that could be made about the ecological importance of horseshoe crabs. One reason for this is that most of the pertinent studies in the literature have been about L. polyphemus, with far fewer reports about Tachypleus tridentatus, T. gigas, and Carcinoscorpius rotundicauda. Of the ecological studies with L. polyphemus, most have been conducted on populations in the middle Atlantic and southern New England. There is also relatively little published information about the feeding ecology of juvenile horseshoe crabs and virtually nothing about the importance of predation on juveniles. It is worth emphasizing that other aspects of horseshoe crab behavior, such as the correlation between spawning intensity and the lunar and tidal cycle, are highly variable across the species range. For example, Barlow et al. (1986) found that spawning intensity in Cape Cod, Massachusetts was timed to coincide with the higher of the two daily high tides and that the highest peaks occurred on the spring tides (near the new moon and full moon). By contrast, in Delaware Bay the spring tide peaks may be disrupted by wind events and/or cold fronts that force the animals offshore until the return of favorable conditions (Shuster and Botton 1985, Smith and Michels 2006), and spawning in the Indian River Lagoon, Florida showed no relationship at all to the lunar cycle (Ehlinger et al. 2003). Given the extreme plasticity in spawning behavior, I would expect that there is geographic variation in feeding behavior and other aspects of the ecology as well. So, there is considerable danger in trying to generalize from the relatively few ecological studies of L. polyphemus in locations such as Delaware Bay and Cape Cod to other portions of its range, much less to the three other species. We are in the somewhat tenuous position of extrapolating the ecological importance of a group of animals whose abundance has already declined substantially, what Pauly (1995) has referred to as the shifting baseline syndrome. In other words, we risk misinterpreting the current situation as the norm, when in fact horseshoe crabs may have already been reduced to a small fraction of their historic abundances. For example, peaks in the Delaware Bay population that occurred during the nineteenth century may be imperfectly documented (Shuster 2003), but, in the writer s opinion, are suggestive of

3 A Review and Speculative Summary 47 abundances far greater than any living scientist has witnessed. An even more extreme situation exists with T. tridentatus along the Seto Inland Sea in Japan, which have been reduced over the past century to the extent that some local populations are extinct (Tsuchiya 2009). The shifting baseline concept extends beyond the population level, in that the ecological importance of horseshoe crabs as predators, for example, is related to the collective impact of the population, so simply knowing what individual crabs eat is not enough to deduce the importance of these predators to the community. 2 Horseshoe Crabs as Predators 2.1 Predation by Adults Adult horseshoe crabs are omnivorous, feeding on a wide variety of benthic invertebrates, including bivalves, polychaetes, crustaceans, and gastropods. The functional morphology of feeding and the anatomy and physiology of the digestive system has recently been reviewed by Botton and Shuster (2003), so this contribution emphasizes the ecological importance of horseshoe crab predation on estuarine and coastal benthic communities. L. polyphemus on the mid-atlantic continental shelf primarily feed on bivalves including blue mussels (Mytilus edulis) and surf clams (Spisula solidissima) (Botton and Haskin 1984; Botton and Ropes 1989). When crabs encounter patches of preferred prey such as thin-shelled bivalves, they may feed extensively, literally packing their guts with shells (Fig. 1). Prey selection has been demonstrated in laboratory feeding experiments (Botton 1984a), where crabs exhibited a clear preference for thinshelled bivalves (e.g., dwarf surf clams, Mulinia lateralis or soft-shell clams, Mya arenaria) when given a choice between these and thicker shelled species, Fig. 1 A longitudinal section through a horseshoe crab showing the anterior portion of the digestive system (mouth, proventriculus or gizzard, and intestine). Note the presence of broken blue mussel shells (Mytilus edulis) in the intestine. Courtesy of Carl N. Shuster

4 48 M.L. Botton including quahogs (Mercenaria mercenaria) and gem clams (Gemma gemma). Bivalves were the most important macrobenthic prey in the stomachs of adult L. polyphemus feeding on a Delaware Bay tidal flat during the breeding season (Botton 1984a), and this was true as well for T. gigas from India (Debnath et al. 1989). Both of these studies found that many animals contained sand, plant detritus, and minute food items such as Foraminifera and nematodes. Botton and Shuster (2003) suggested that when preferred prey are rare, horseshoe crabs may ingest sediment rather indiscriminately, which would account for the presence of such minutely sized food items. The horseshoe crab digestive system contains the enzyme cellulase (Debnath et al. 1989) demonstrating that the plant detritus may be nutritionally useful. The ecological importance of adult horseshoe crabs as predators has primarily been studied on intertidal sand bars and mud flats during the breeding season. Horseshoe crabs withdraw to these areas after spawning on the beaches at high tide, and while they await the return of the tide, they dig pits in search of food or to avoid desiccation. Predator exclusion techniques (caging experiments) have been used to assess the ecological importance of predation by adult horseshoe crabs in these habitats. The first of these studies was conducted in Massachusetts in response to assertions from commercial fishermen that predation was causing enormous destruction to planted soft-shell clams. Plots that were caged to exclude predators had significantly higher clam survival than uncaged plots (Smith and Chin 1951; Smith et al. 1955). Many of the young-of-the-year clams within the caged areas achieved sizes of more than 20 mm by September, but no clams above 10 mm survived in the uncaged areas. Botton (1984b) demonstrated similar impacts of predation in an exclusion study on Delaware Bay tidal flats. There was substantial recruitment of small M. lateralis and M. arenaria into both caged and uncaged plots in June By August, there were few clams above 4 mm outside the predator exclosures, whereas Mulinia and Mya protected from predation grew to lengths of mm. Aside from these dramatic effects on bivalve survival and growth, Botton (1984b) found that the exclusion of predators led to significant increases in total invertebrate abundance, biomass, and species diversity (average number species per core) than unprotected sediments. In any predator exclusion study, it is difficult to ascertain the extent to which the target predator caused the response. Smith and Chin (1951) noted that the tidal flats were riddled with horseshoe crab pits and also found shell fragments of Mya and other bivalves in horseshoe crab guts and fecal pellets. However, other clam predators such as the green crab (Carcinus maenas) werealsoexcludedbycertain caging treatments. Botton s (1984b) inference that horseshoe crab predation was responsible for most of the effects seen in his caging experiment was corroborated by a study of gut contents and aquarium feeding trials, which confirmed that horseshoe crabs in this habitat preferentially consumed thin-shelled bivalves such as Mulinia and Mya (Botton 1984a). Furthermore, a manipulation using a toponly (floating mesh) design that was specifically designed to exclude predatory gulls and shorebirds showed that bird exclusion had minimal effects on the benthic community in comparison to the full cages (Botton 1984c).

5 A Review and Speculative Summary 49 The potential impacts of horseshoe crabs as predators are intertwined with their effects as sediment disturbers, and predator exclusion studies cannot readily differentiate between the importance of sediment disturbance versus predation. In the case of horseshoe crabs, both effects may be relevant. Kraeuter and Fegley (1994) found that portions of a Delaware Bay tidal flat that were subjected to horseshoe crab burrowing were disturbed to a mean depth of 11.1 cm, whereas areas that were caged to exclude horseshoe crabs were reworked (by waves and currents) to just 3.2 cm. The intense sediment reworking by horseshoe crabs could impact prey by crushing them or bringing them to the surface, where they may be consumed by predators such as gulls. The most common invertebrate on these tidal flats is the gem clam, G. gemma, which has a hard shell that makes it resistant to predation and disturbance. Comitto et al. (1995) studied the recolonization of Limulus pits and found that Gemma generally recovered within 1 day after disturbance events. A significant amount of sediment disturbance by horseshoe crabs also occurs during egg deposition (Jackson et al. 2005; Nordstrom et al. 2006; Smith 2007), and this may be an extremely important mechanism by which eggs in deep sediments are moved to the sediment surface where they are accessible to foraging shorebirds (see Section 3.1.1). In summary, it is clear that dense aggregations of adult L. polyphemus have ecologically significant impacts on invertebrate populations on nearshore mud flats and sand bars, related to feeding and/or sediment disturbance. With the onset of cooler temperatures, the crabs disperse into deeper waters where much less is known about their ecological importance. There is virtually no available data on the feeding ecology of L. polyphemus in northern New England, or anywhere south of Virginia, and the paucity of information on the three Asian species is also noteworthy. 2.2 Predation by Juveniles The trilobite larvae subsist on the yolk; independent feeding does not begin until the second instar stage. The digestive system in juvenile crabs is fully differentiated into discrete regions of mouth, esophagus, proventriculus, intestine, rectum, and anus (Shuster 1948). However, the size and crushing ability of the feeding appendages (see Botton and Shuster 2003) constrains the choice of foods in the smallest size classes of horseshoe crabs. Not surprisingly, then, the diets of these animals shift as they grow larger. The diets of various sizes of T. gigas in the Bay of Bengal over a year-long period were reported by Chatterji et al. (1992). Important prey included mollusks, insects and crustaceans, and polychaetes. Decayed organic material, sand, and plant detritus were highest from July to October, coinciding with the period of time when preferred molluscan species were lowest. Crabs < 120 mm carapace length (CL) consumed less food than crabs > 141 mm CL. Zhou and Morton (2004) enumerated the gut contents of nine juvenile T. tridentatus between 8.5 and 67 mm prosoma width (PW) and two C. rotundicauda between 50 and 52 mm PW from tidal flats in Hong Kong. Based on this limited sample

6 50 M.L. Botton Table 1 Estimated maximum percentage of potential prey items in the mixed diet of juvenile horseshoe crabs at Nauset Beach, Massachusetts based on stable isotope signatures Instar number Prey category Bivalves ND ND Gastropods ND ND Crustaceans/polychaetes ND ND Benthic POM 21 < Suspended POM 100 < POM ¼ particulate organic material, ND ¼ not detected. Modified from Gaines et al. (2002). size, the diets of the two species were similar, and insect larvae were the most common food item. Polychaetes, oligochaetes, small crabs and other crustaceans, and thin-shelled bivalves were also eaten. Gaines et al. (2002) and Carmichael et al. (2004) used stable isotopes to study the feeding ecology of juvenile L. polyphemus from Massachusetts. Comparisons of nitrogen and carbon isotopic signatures of horseshoe crab tissues with potential prey in the estuary are useful in deducing the trophic position of the animals in the food web. The nutrition of second and third instars was largely derived from benthic and suspended particulate organic material, originating from phytoplankton, macroalgae, and salt marsh (Spartina alterniflora) production in second instars, but mainly from Spartina in third instars (Gaines et al. 2002). Gradually, the older juveniles became progressively more reliant on crustaceans, polychaetes, and mollusks (Table 1). The stable isotope technique also enabled Carmichael et al. (2004) to trace back the locations where juvenile crabs had been feeding to sub-estuaries that differed in nitrogen loading. 3 Horseshoe Crabs as Prey 3.1 Eggs, Trilobite Larvae, and Juveniles Predation by Birds The importance of horseshoe crab eggs as food for migratory shorebirds in Delaware Bay has now been very well established and is reviewed by Mizrahi and Peters (2009). Early evidence linking horseshoe crab eggs and shorebirds was based primarily on observational data (e.g., Botton et al. 1994), further supported by Tsipoura and Burger (1999) who found that shorebird stomach contents were dominated by Limulus eggs. There are strong relationships between the density of horseshoe crab eggs and the abundance of red knots along the Delaware Bay shore (Karpanty et al. 2006). Perhaps most persuasively, Haramis et al. (2007) showed that free-ranging shorebirds collected from Delaware Bay had d15 N signatures that were identical with the d15 N signatures of captive shorebirds that were fed a diet of horseshoe crab eggs alone.

7 A Review and Speculative Summary 51 Shorebirds feed on prodigious quantities of horseshoe crab eggs during their stopover on Delaware Bay. Castro et al. (1989) estimated a daily consumption of 8,300 eggs by sanderlings (Calidris alba). Haramis et al. (2007) estimated that red knots (C. canutus) eat an average of 18,350 eggs/day during the period of maximum feeding, with a peak daily consumption of 23,940 eggs, while ruddy turnstones (Arenaria interpres) ate an average of 13,300 eggs/day with a peak daily consumption of 19,360 eggs. These remarkable daily rations are required to achieve the increases in body mass that are needed for the northbound flight to the Arctic breeding areas. Shorebirds foraging on eggs at the sediment surface feed by pecking at rapid rates, ranging from 1.2 pecks/s for ruddy turnstones to 2.4 pecks/s for sanderlings (Gillings et al. 2007). Haramis et al. (2007) deduced that red knots need to eat about 5,000 eggs in order to gain 1 g of mass. Since each red knot gains about 80 g mass during its stay in Delaware Bay, it follows that each bird would need to eat roughly 400,000 eggs. Hence, a population of 40,000 red knots would need to eat approximately 16 billion eggs. At the present time, only a minority of Delaware Bay beaches have sufficient densities of crab eggs to attract flocks of red knots (Karpanty et al. 2006), and the inability of red knots to find adequate food throughout the bay may be having serious effects on their survival (Baker et al. 2004). Clearly, horseshoe crab eggs are vital for shorebirds in Delaware Bay, but does bird predation have a significant impact on the total numbers of horseshoe crab eggs deposited by female crabs? Gillings et al. (2007) demonstrated that shorebirds feeding on horseshoe crabs eggs in sand-filled trays could cause shortterm depletion of surface eggs. However, for the large number of shorebirds that feed in the swash zone (Botton et al. 1994), eggs are continually being replenished by wave action (Nordstrom et al. 2006), and wave periods (ca s) are probably sufficiently rapid to neutralize the effects of shorebird foraging on surface egg density. Moreover, the deep sediments that contain most of the fresh egg clutches are extensively reworked by successive spawning events during both of the two daily high tides. It is this process of exhumation that ultimately brings most of the eggs toward the surface where they are available to birds (Smith 2007), because wave action during typical spring conditions in Delaware Bay causes much less disturbance to the sediment than the spawning process itself (Jackson et al. 2005). These processes would indicate that depletion of surface eggs by foraging shorebirds, as suggested by the work of Gillings et al. (2007), may only apply to those birds feeding on dry sand above the swash zone. I would propose that shorebird predation on horseshoe crab eggs in Delaware Bay is far more important to the birds than it is as a potential limiting factor for the crabs. Eggs that are left on the surface litter lines by the receding tide (as described by Nordstrom et al. 2006) will desiccate and die if they are not consumed by predators. Moreover, the density of eggs in the upper 5 cm of the beach is generally 10% or less than the egg densities at depths of 5 20 cm (Botton et al. 1994). In addition, the annual peaks in horseshoe crab spawning abundance do not always coincide with the peak of the shorebird migration, because cold water temperatures and/or unfavorable wind and wave conditions

8 52 M.L. Botton can cause the crabs to delay spawning (Shuster and Botton 1985, Smith and Michels 2006). Eggs deposited in June have a smaller risk of predation, since most shorebirds depart the bay shore by the end of May (Clark et al. 1993). Beyond the Delaware Bay area, the quantitative importance of bird predation on horseshoe crab eggs is largely unproven, although the interaction has been noted in locations such as Plymouth Bay, Massachusetts (Mallory and Schneider 1979), Jamaica Bay, New York (Riepe 2001), Sandy Hook Bay, New Jersey (Loveland and Botton unpublished), and Great Bay, New Jersey (Sullivan 1986). On Cape Cod, Massachusetts beaches, densities of horseshoe crab eggs are generally <10,000 m 2, and mainly occur at depths <5 cm (James-Pirri et al. 2005). It is questionable whether such low egg densities would make it profitable for shorebirds to specialize on this resource, nor is it known whether bird predation is a major cause of mortality for crab eggs Predation by Fish and Crustaceans There is very little quantitative information about the importance of fishes and benthic predators to horseshoe crab eggs and larvae. Feeding by the sand shrimp, Crangon septemspinosa, juvenile blue crabs (Callinectes sapidus) and spider crabs (Libinia sp.), and by various surf zone fishes such as eels, catfish, juvenile striped bass, white perch, killifish, weakfish, and Atlantic silversides has been observed (Warwell 1897; Perry 1931; desylva et al. 1962; Price 1962; Spraker and Austin 1997; Botton and Loveland unpublished). In Delaware Bay, New Jersey, killifish (Fundulus heteroclitus) and Atlantic silversides (Menidia menidia) are the two most common fishes caught near tidal creeks where horseshoe crabs frequently spawn (Botton and Loveland, unpublished). In August 2001, horseshoe crab eggs or trilobites occurred in the stomachs of 95% of the killifish and 96% of the Atlantic silversides (Table 2). Individual fish had up to 34 eggs and 51 trilobites in their stomach. Menidia consumed more eggs than Fundulus, although the difference was non-significant (2-tailed t-test, t 43 = 0.35). Conversely, Fundulus consumed more trilobite larvae than Menidia, with the difference being marginally significant (t 43 =1.94, p = 0.06). Overall, Fundulus consumed an average of 16.9 horseshoe crab eggs and larvae, and Menidia, 11.5(t 43 =1.34,p = 0.19). A previous study on Menidia indicated that trilobites, which were abundant in the guts just after Table 2 Predation by killifish (Fundulus heteroclitus, n=20) and Atlantic silversides (Menidia menidia, n=25) on horseshoe crab eggs and trilobite larvae, based on a sample of fish collected on August 22, 2001, from a tidal creek at Kimbles Beach, Delaware Bay, NJ Frequency of occurrence Mean (SD) per gut Species of fish Mean TL Eggs Trilobites Total stages Eggs Trilobites Total stages Killifish % 95% 95% 2.8 (7.6) 14.1 (11.7) 16.9 (15.1) Atlantic silversides % 92% 96% 3.5 (5.0) 8.0 (8.6) 11.5 (11.0) TL = total length, SD = standard deviation.

9 A Review and Speculative Summary 53 midnight (0015 hours), were completely evacuated by 0645 hours (Spraker and Austin 1997). If similar gut passage times apply to the fish collected from Delaware Bay that would indicate the potential for Atlantic silversides and killifish to have a daily ration of about 46 and 68 Limulus daily, respectively. Hermit crabs (Pagurus longicarpus) are abundant on Delaware Bay tidal flats throughout the spring and summer, generally occupying shells of mud snails (Ilyanassa obsoleta) or Atlantic oyster drills (Urosalpinx cinerea). We sampled the hermit crab population by taking a series of 15 replicate 1 m 2 quadrats on each of the first 5 sand bars on the intertidal flats, a distance approximately 200 m offshore. This region includes about 80 90% of the young-of-the-year horseshoe crab population on the flats (Botton et al. 2003). About 75% of the hermit crabs were in the small size class (total claw length mm), and nearly the entire remainder were medium sized ( mm). Total hermit crab densities ranged from about 2.7 to 7.2 animals m 2 on July 20, and about 1.7 to 4.1 m 2 on July (Fig. 2). By comparison, Botton et al. (2003) enumerated about 10 trilobites m 2, 2 3 second instars m 2, and < 1 third instar m 2 on the same tidal flats at the same time that these hermit crab surveys were conducted. Behavioral observations of predation by P. longicarpus on Limulus trilobites and second instars in aquaria indicated that the hermit crabs attacked the ventral surface, using their claws to pick out portions of the legs and gills. Most of the chitinous tissue, including virtually all of the prosoma and opisthosoma, was not ingested. We therefore felt that stomach contents would not be a reliable measure of hermit crab predation. Instead, we tested individual hermit crabs in aquaria with known numbers of trilobites or second instars, sieved the sand after an 8 12 hour feeding interval, and then counted the remaining horseshoe crabs. The percent recovery of horseshoe crabs in the absence of a hermit crab predator was 99% (average of 52 replicates), indicating that there were no other significant losses that took place during the procedures. Fig. 2 Mean number of hermit crabs across a Delaware Bay intertidal sand flat, July Bar 1 is closest to shore and bar 5 is approximately 200 m from shore. Fifteen replicate 1 m 2 quadrats were taken on each of the five sand bars on each date. Hermit crabs were grouped into three size classes based on total claw length (i.e., combined length of the dactyl and propodus): small ( mm), medium ( mm), and large (> 8.0 mm)

10 54 M.L. Botton Hermit crabs preyed on both trilobites and second instars. Among the small hermit crabs, 76.7% ate at least one trilobite, with an average predation rate of 0.33 per hour. Fourteen of 15 medium hermit crabs fed on at least one trilobite (93.3%), and the average predation rate was about three times higher, 1.12 per hour. Among the large hermit crabs, 13 of 15 fed on at least one trilobite (86.7%) and the average predation rate was 1.07 per hour. There was a statistically significant difference in predation rate between the small and both the medium and large size classes, but no difference between the medium and large size classes (1-way ANOVA, F 2,57 =79.7,p < followed by post hoc Bonferroni multiple comparisons test). In 94 feeding trials in which small hermit crabs were put in aquaria with second instars, 85.1% consumed at least 1 second instar, with an average predation rate of 0.41 per hour (Fig. 3). Among medium hermit crabs (n=61), 98.4% ate at least 1 second instar and the average predation rate was about doubled (0.83 per hour). Virtually all (98.0%) of the large hermit crabs fed (n = 50), and the average predation rate was 0.91 per hour. The predation rate by small hermit crabs was significantly smaller than both the medium and large size classes, but there was no difference in feeding rates between the medium and large size classes (1-way ANOVA, F 2,204 =16.88,p < 0.001). There were no statistically significant differences in predation rates on trilobites versus second instars for any of the three size classes of hermit crabs. The net impact of hermit crab predation can be approximated by multiplying the predation rates for each size class by the densities of each size class on the intertidal flats (Table 3). Although the feeding rate per individual was lowest among small hermit crabs, they had the greatest numerical impact on horseshoe Fig. 3 Predation by hermit crabs on second instar horseshoe crabs based on aquarium feeding trials conducted on 15 dates between August and October Aquaria were cm, and had a 1 cm layer of clean sand covered by 1.5 cm of filtered bay water. Hermit crabs were grouped into three size classes as defined in Fig. 2: small (n = 94), medium (n = 61), and large ( n = 50). Second instars (initial n = 30 or 40) were given 30 minutes to acclimate and burrow before the hermit crab was added and allowed to feed for 8 or 12 hours. Feeding rates were normalized to the number of second instars eaten per hour; since feeding rates in 8 or 12 hour trials were not significantly different, the data were pooled

11 A Review and Speculative Summary 55 Table 3 The net impact of hermit crab predation on trilobites and second instars on intertidal sand flats in Delaware Bay, NJ Mean predation rate (no./day) July 20 July Hermit crab size class Trilobites Second instars Hermit crab density Predation rate on trilobites hermit crab density Predation rate on Second instars hermit crab density Hermit crab density Predation rate on trilobites hermit crab density Small Medium Large Predation rate on second instars hermit crab density

12 56 M.L. Botton crabs on July 20 because they were much more numerous than medium and large hermit crabs. On July 27 28, medium hermit crabs had a slightly larger impact on trilobites, but the reverse was true for second instars. A better understanding of the quantitative importance of predation on young-of-the-year and juvenile horseshoe crabs is needed if we are to have a better understanding of recruitment processes in natural populations (Botton et al. 2003; Grady and Valiela 2006). The limited amount of information from Delaware Bay, NJ, and Pleasant Bay, MA, suggests that there is very high mortality from eggs through the end of the first summer of life (Carmichael et al. 2003; Botton et al. 2003). There is also a growing interest in the feasibility of utilizing aquaculture as a means of enhancing stocks of horseshoe crabs. Fertilized eggs would be reared in the laboratory for eventual release into the field as juveniles (e.g., Mishra 2009, Schreibman and Zarnoch 2009). For this to be successful, we must have much more information about the causes and magnitude of stage-specific mortality. However, we currently lack data on the causes and magnitude of natural mortality for horseshoe crabs between the early instars and maturity. 4 Adult Horseshoe Crabs as Prey Mortality of adult horseshoe crabs, caused by natural factors and fisheries, does not have the same importance to the population growth rate as does the survival of juveniles (Grady and Valiela 2006). The large size and dense exoskeleton of adult horseshoe crabs certainly protects them against most predators, and adult horseshoe crabs are not consumed with any regularity by most known predators (Botton and Shuster 2003). However, a number of interesting examples of adult mortality are known which may be important to particular populations of horseshoe crabs. Reid and Bonde (1990) and Ehlinger (personal communication) have observed large American alligators (Alligator mississippiensis) eating adult L. polyphemus on multiple occasions in the Indian River Lagoon, Florida. Adult horseshoe crabs are a significant component of the stomach contents of loggerhead turtles (Caretta caretta) in lower Chesapeake Bay (reviewed by Keinath 2003). Interestingly, the diet of loggerhead turtles in Virginia shifted from horseshoe crabs in the early to mid-1980s to blue crabs (C. sapidus) in the late 1980s, and then more recently to finfish (Seney and Musick 2007). These shifts in stomach contents were probably triggered by declines in the horseshoe crab and blue crab fisheries, respectively; moreover, the declines in horseshoe crabs and blue crabs may be linked with the decrease in the number of sea turtles in the lower Chesapeake Bay over the past two decades. Using aerial and net surveys, Spotila et al. (2007) found that sea turtle densities in lower Delaware Bay were comparable to the lower Chesapeake Bay. It has not been determined whether loggerheads in Delaware Bay feed extensively on horseshoe crabs, though this would seem a likely possibility given the high

13 A Review and Speculative Summary 57 density of horseshoe crabs in this location. It is uncertain whether there are other species of sea turtles that feed on horseshoe crabs; Barleycorn and Tucker (2005) observed a Kemp s Ridley turtle (Lepidochelys kempii) eating a horseshoe crab in Charlotte Harbor (Gulf of Mexico), Florida. Adult horseshoe crabs are frequently stranded on beaches during spawning, especially in relatively high-energy estuaries such as Delaware Bay (Botton and Loveland 1989). Predation by large gulls on stranded individuals has been implicated as a significant cause of mortality among stranded adults. Herring gulls (Larus argentatus) and great black-backed gulls (Larus marinus) frequently eat live upside-down horseshoe crabs by tearing out their gills and legs in order to access the eggs and other viscera (Botton and Loveland 1993). The only report of bird predation on any of the three Asian species is from Debnath and Choudhury (1988), who found that crows (Corvus spelendens) ate T. gigas in India. 5 Horseshoe Crabs as Hosts for Epibionts Horseshoe crabs carapaces frequently serve as a substrate for encrusting invertebrates and algae. These associations are neither parasitic nor commensal, and are better described by the term epibiosis (Wahl 1989): a non-symbiotic, facultative association between the substrate organism and sessile animals (epizoans) or algae (epiphytes). Bryozoans, barnacles, tube-building polychaetes, and sessile mollusks such as mussels, oysters, and slipper limpets are among the more conspicuous epibionts on the three species of horseshoe crabs that have been studied, namely T. gigas (Key et al. 1996; Patil and Anil 2000), C. rotundicauda (Key et al. 1996), and L. polyphemus (Allee 1922; Botton and Ropes 1988; Dietl et al. 2000; Botton and Shuster 2003; Grant 2003). Typically, epibionts are generalists in their choices of substrates (Wahl and Mark 1999), and all of the epibionts that attach to horseshoe crabs are widespread on other types of hard substrate. Epibionts living on horseshoe crabs are examples of sessile organisms living on moving substrates (Key et al. 1996). As such, their ecology may differ from their conspecifics that are attached to rocks and other non-moving objects. For example, sessile organisms living on mobile substrates may have enhanced gene dispersal, and filter-feeders may have better feeding opportunities because water flow may be enhanced (Wahl 1989). But because horseshoe crabs are so highly migratory, any organisms living on them must be able to survive the same range of temperatures and salinities as their host. They are also subjected to aerial exposure when the horseshoe crabs come ashore to spawn. When horseshoe crabs become stranded on a beach (Botton and Loveland 1989), the combination of desiccation and high temperature frequently kills epibionts such as the blue mussel (M. edulis) and slipper limpet (Crepidula fornicata) even though the horseshoe crab is still alive (personal observations).

14 58 M.L. Botton For the most part, the associations of horseshoe crabs and epibionts cause little or no damage to the host (Key et al. 1996). Blue mussels sometimes attach to the walking legs and book gills, potentially impeding their function (Botton 1981). The ability of the crabs to obtain sensory input from their lateral eyes may be impeded by overgrowth (Wasserman and Cheng 1996), but an even more severe impact on vision is caused by bacterial and green algal infections that cause the loss of ommatidia, which apparently makes it less likely for males to visually locate females prior to amplexus (Duffy et al. 2006). These and other infestations of horseshoe crabs are discussed by Nolan and Smith (2009). Epibionts have only been reported to occur on adult horseshoe crabs, in part because the frequency of molting (Sekiguchi et al. 1988) precludes the establishment of a fouling community on juveniles. In contrast, adult crabs generally do not molt after reaching sexual maturity (Botton and Ropes 1988). The smooth, glossy carapaces of juvenile and recently molted young adults normally lack epibionts, and the lateral eyes are clear (Duffy et al. 2006). The absence of epibionts in juveniles and young adults may be related to the secretion of a mucus with anti-fouling properties (Patil and Anil 2000; Harrington and Armstrong 2000). 6 Summary and Conclusions Predation and sediment disturbance by adult horseshoe crabs can be ecologically significant phenomena where the animals are concentrated in large numbers. A good demonstration of the importance of considering the size of the horseshoe crab population in inferring the magnitude of an ecological process is the study by Smith (2007), who showed that the quantity of L. polyphemus eggs exhumed from beach sediments by horseshoe crab digging was dependent on the number of spawners. It is reasonable to assume that there are similar density-dependent relationships between horseshoe crabs and sediment disturbance on intertidal flats (Kraeuter and Fegley 1994) and between horseshoe crab predation and the effects on benthic infauna (Botton 1984b). To date, the ecological impacts of horseshoe crabs as sediment disturbers and predators have been evaluated only where crabs are most numerous, most notably Delaware Bay. There is a need for similar studies elsewhere, and in particular, for the three Asian species. The greatly diminished number of horseshoe crabs in Japan and elsewhere in southeast Asia limits our ability to infer the importance that these animals may have had in previous generations (Pauly 1995). Since the review by Botton and Shuster (2003), there have been several papers adding to our understanding of the distribution and feeding ecology of juvenile horseshoe crabs (Botton et al. 2003; Zhou and Morton 2004; Carmichael et al. 2004), and advances on raising horseshoe crab juveniles in captivity (Carmichael et al. 2009, Schreibman and Zarnoch 2009) also give important insights into the trophic position of juvenile crabs. Stable isotope

15 A Review and Speculative Summary 59 techniques have revealed that juvenile horseshoe crabs show dramatic ontogenetic shifts in their choices of food, and may move between different areas within an estuary (Gaines et al. 2002; Carmichael et al. 2004). As with adults, understanding the significance of juvenile horseshoe crabs in the flow of energy through the ecosystem depends on knowing their abundance as well as their individual feeding habits. We are beginning to understand that juvenile horseshoe crabs may be abundant in subtidal areas (Burton et al. 2009), where little is known about their role as predators. Studies coupling juvenile abundance and feeding would contribute much to our understanding of horseshoe crab ecology. The nutritional significance of the horseshoe crab eggs for migratory shorebirds in Delaware Bay has been extensively documented (Botton et al 2003; Mizrahi and Peters 2009), but it is not clear whether horseshoe crab eggs are more than incidental food for birds in other coastal areas. Although shorebirds consume vast number of eggs during their stopover, I suggest that because shorebirds feed mainly on eggs at the sediment surface, they are eating eggs that would probably desiccate and die if they were not eaten. I do not believe that we understand enough about the numerical relationships between egg abundance, juvenile survival, and adult recruitment to infer that bird predation in Delaware Bay is presently limiting the size of the horseshoe crab population, but I would consider this very unlikely. Loggerhead turtles (C. caretta) may be the only predator with a substantial consumption of adult horseshoe crabs, and it is notable that temporal shifts in their food preference from Limulus to blue crabs and fishes coincided with a decreased population of horseshoe crabs in Virginia (Seney and Musick 2007). We do not yet know whether significant consumption of horseshoe crabs by sea turtles occurs outside of the lower Chesapeake Bay. Because sea turtles are endangered, a better understanding of their interactions with horseshoe crabs is needed. Apart from some limited information about predation by fish (Table 2) and hermit crabs (Fig. 3 and Table 3), there is virtually no data on predation rates on trilobites and second instars. Even less is known about predation and other ecological factors affecting the survival of older juveniles. These are clearly vital gaps in our understanding of horseshoe crab ecology, with potentially important implications for understanding recruitment dynamics (Grady and Valiela 2006). References Allee WC (1922) Studies in marine biology II: An annotated catalog of the distribution of common invertebrates in the Woods Hole littoral. Unpublished manuscript in the Marine Biological Laboratory Library, Woods Hole, MA Baker AJ, Gonza lez PM, Piersma T, Niles LJ, de Lima do Nascimento I, Atkinson PW, Clark NA, Minton CDT, Peck MK, Aarts G (2004) Rapid population decline in red knots: fitness consequences of decreased refuelling rates and late arrival in Delaware Bay. Proc Biol Sci 271: Barleycorn AA, Tucker AD (2005) Lepidochelys kempii (Kemp s Ridley seaturtle) diet. Herpetol Rev 36: 8 9

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